Zoonotic transmission of Teladorsagia circumcincta and Trichostrongylus species in Guilan province, northern Iran: molecular and morphological characterizations.

BACKGROUND: Parasitic trichostrongyloid nematodes have a worldwide distribution in ruminants and frequently have been reported from humans in Middle and Far East, particularly in rural communities with poor personal hygiene and close cohabitation with herbivorous animals. Different species of the genus Trichostrongylus are the most common trichostrongyloids in humans in endemic areas. Also, Ostertagia species are gastrointestinal nematodes that mainly infect cattle, sheep and goats and in rare occasion humans. The aim of the present study was to identify the trichostrongyloid nematodes obtained from a familial infection in Guilan province, northern Iran, using morphological and molecular criteria. METHODS: After anthelmintic treatment, all fecal materials of the patients were collected up to 48 h and male adult worms were isolated. Morphological identification of the adult worms was performed using valid nematode keys. Genomic DNA was extracted from one male worm of each species. PCR amplification of ITS2-rDNA region was carried out, and products were sequenced. Phylogenetic analysis of the nucleotide sequence data was performed using MEGA 6.0 software. RESULTS: Adult worms expelled from the patients were identified as T. colubriformis, T. vitrinus and Teladorsagia circumcincta based on morphological characteristics of the males. Phylogenetic analysis illustrated that each species obtained in current study was placed together with reference sequences submitted to GenBank database. CONCLUSIONS: The finding of current study confirms the zoonotic aspect of Trichostrongylus species and T. circumcincta in inhabitants of Guilan province. The occurrence of natural human infection by T. circumcincta is reported for the first time in Iran and the second time in the world.

Host immunity shapes the impact of climate changes on the dynamics of parasite infections.

Global climate change is predicted to alter the distribution and dynamics of soil-transmitted helminth infections, and yet host immunity can also influence the impact of warming on host-parasite interactions and mitigate the long-term effects. We used time-series data from two helminth species of a natural herbivore and investigated the contribution of climate change and immunity on the long-term and seasonal dynamics of infection. We provide evidence that climate warming increases the availability of infective stages of both helminth species and the proportional increase in the intensity of infection for the helminth not regulated by immunity. In contrast, there is no significant long-term positive trend in the intensity for the immune-controlled helminth, as immunity reduces the net outcome of climate on parasite dynamics. Even so, hosts experienced higher infections of this helminth at an earlier age during critical months in the warmer years. Immunity can alleviate the expected long-term effect of climate on parasite infections but can also shift the seasonal peak of infection toward the younger individuals.

Parasitized mates increase infection risk for partners.

Individuals can gain fitness benefits and costs through their mates. However, studies on sexual selection have tended to focus on genetic benefits. A potentially widespread cost of pairing with a parasitized mate is that doing so will increase an individual's parasite abundance. Such a cost has been overlooked in systems in which parasites are indirectly transmitted. We manipulated the abundance of the nematode parasite Trichostrongylus tenuis, an indirectly transmitted parasite, within pairs of wild red grouse Lagopus lagopus scoticus in spring. Parasite levels were correlated within pairs before the experiment. We removed parasites from males, females, or both members of the pair and evaluated individual parasite uptake over the subsequent breeding period. At the end of the breeding season, an individual's parasite abundance was greater when its mate had not been initially purged of parasites. This cost appeared to be greater for males. We discuss the implications of our results in relation to the costs that parasites may have on sexual selection processes.

Peak shift and epidemiology in a seasonal host-nematode system.

Insight into the dynamics of parasite-host relationships of higher vertebrates requires an understanding of two important features: the nature of transmission and the development of acquired immunity in the host. A dominant hypothesis proposes that acquired immunity develops with the cumulative exposure to infection, and consequently predicts a negative relationship between peak intensity of infection and host age at this peak. Although previous studies have found evidence to support this hypothesis through between-population comparisons, these results are confounded by spatial effects. In this study, we examined the dynamics of infection of the nematode Trichostrongylus retortaeformis within a natural population of rabbits sampled monthly for 26 years. The rabbit age structure was reconstructed using body mass as a proxy for age, and the host age-parasite intensity relationship was examined for each rabbit cohort born from February to August. The age-intensity curves exhibited a typical concave shape, and a significant negative relationship was found between peak intensity of infection and host age at this peak. Adult females showed a distinct periparturient rise in T. retortaeformis infection, with higher intensities in breeding adult females than adult males and non-breeding females. These findings are consistent with the hypothesis of an acquired immune response of the host to a parasite infection, supporting the principle that acquired immunity can be modelled using the cumulative exposure to infection. These findings also show that seasonality can be an important driver of host-parasite interactions.

Spatial parasite transmission, drug resistance, and the spread of rare genes.

The transmission of many parasitic worms involves aggregated movement between hosts of "packets" of infectious larvae. We use a generic metapopulation model to show that this aggregation naturally promotes the preferential spread of rare recessive genes, compared with the expectations of traditional nonspatial models. A more biologically realistic model also demonstrates that this effect could explain the rapid observed spread of recessive or weakly dominant drug-resistant genotypes in nematode parasites of sheep. This promotion of a recessive trait arises from a novel mechanism of inbreeding arising from the metapopulation dynamics of transmission.

The development of Trichostrongylus colubriformis larvae on a range of herbage species or on plots of differing topographical aspect.

Five "contaminations", where faeces containing Trichostrongylus colubriformis eggs were deposited on pasture and serially recovered, were used to compare the rate of decline of faecal mass and larval development. In the first three contaminations, faeces from a common source were deposited on swards of browntop (Agrostis capillaris cv Grasslands Muster), ryegrass (Lolium perenne cv Grassland Nui), white clover (Trifolium pratense cv Grassland Tahora), or onto bare ground in the late spring, summer or autumn. The last two contaminations were done on the north facing aspect or south facing aspect of hill country pastures in summer and autumn. Number of free-living nematodes (first- and second-stage larvae (L(1) and L(2)) and soil dwelling nematodes) and third stage larvae (L(3)) recovered from faeces were counted. In spring there was a significant (P<0.01) effect of sward type on the mass of faeces remaining, with greatest mass remaining on browntop and ryegrass 28 days later, and less on bare ground and white clover. In summer there were more (P<0.05) faeces remaining on browntop than on other herbages which had little faeces remaining and which did not differ one from another. In autumn there was a rapid decline in faecal mass. All faeces were gone from white clover and ryegrass swards by day 10 and from browntop and bare ground by day 14. The number of free-living nematodes did not differ markedly between seasons, ranging from 5 to 8.5% of eggs deposited. The number of L(3) recovered was low in spring ( approximately 0.4% of eggs deposited) and did not differ between swards. In summer, more (P<0.05) L(3) were recovered from faeces deposited on swards of ryegrass and white clover than from bare ground or browntop. Most L(3) were recovered from days 7 to 14 ( approximately 1.3% of eggs deposited). In the autumn, low numbers of L(3) were recovered from browntop on day 3 and ryegrass on day 7 (0.2% of eggs deposited) with virtually no L(3) recovered from faeces placed on white clover or bare ground. There were significant (P<0.001) effects of aspect on the amount of faecal mass remaining in both summer and autumn with less faeces remaining on the south facing aspect than on the north. This was particularly evident during the summer when virtually all of the faeces were intact on the north facing aspect but only 40% was remaining on the south on day 28. In the autumn, while faeces were completely gone from both aspects by day 28 but there were less (P<0.05) faeces remaining on the south facing aspect from days 3 to 18 than from the north. There was no aspect effect in either season on the number of free-living nematodes recovered which averaged 8-11% of eggs deposited. In both seasons a greater number of L(3) were recovered from faeces on the south facing aspect than on the north, particularly 3-10 days after faecal deposition. In summer the rise in L(3) recovered in faeces was more rapid on south facing aspect than on the north but both attained a maximum level of approximately 4% of eggs deposited. In autumn on day 3 there was a rapid rise on south facing aspect to approximately 21% of eggs deposited followed by a gradual decline on day 10 while on the north facing aspect numbers of L(3) recovered only attained 10% of eggs deposited.

Effect of topographical aspect and farm system on the population dynamics of Trichostrongylus larvae on a hill pasture.

The population dynamics of Trichostrongylus colubriformis larvae were compared over two years on contrasting topographical aspects north (warm and dry) and south-facing (cool and moist) hill slopes) on paddocks which form part of the 'non-chemical' and conventional' farm systems at the AgResearch Ballantrae Hill Country Station located in a summer-moist region of New Zealand. Sheep faeces containing 50,000 Trichostrongylus eggs were incubated for 4 days at 25 degrees C and then deposited on each of 36 sub-plots in each of 8 plots in a 2 x 2 factorial design in the summer (summer trial) and again in autumn (autumn trial). Pasture was removed to ground level and larvae extracted from six sub-plots from each plot 2, 4, 6, 8, 11 and 14 weeks after contamination in all trials. Larvae were recovered from two strata, 0-5 cm above the soil surface and > 5 cm above the soil surface. Fewer (p < 0.001) larvae were recovered from herbage (47 vs. 118) and residual faeces (28 vs. 246) from the autumn than from the summer trials. This coincided with more rapid (p < 0.001) faecal disappearance in the autumn trials. In the summer trials, fewer (p < 0.003) larvae were recovered from the herbage (101 vs. 182) and residual faeces (140 vs. 352) from plots on the south than the north facing aspect. In the autumn trials there was a rapid (p < 0.0001) faecal disappearance from the south-facing aspect. In the autumn trials there was a non-significant (p < 0.10) trend for fewer larvae to be recovered from the south-facing aspect (2 vs. 54). This also coincided with more rapid faecal disappearance from the south-facing aspect. There was no effect of farm system on the number of larvae recovered. Despite greater (p < 0.0001) numbers of larvae recovered from the bottom stratum of herbage, the density of larvae (L3/kg DM) tended (p < 0.12) to be higher in the top stratum of herbage. It was concluded that season and aspect have a marked effect on the number of larvae recovered from herbage and that this was inversely related to the rate of faecal disappearance.

Transmission dynamics and host-parasite interactions of Trichostrongylus tenuis in red grouse (Lagopus lagopus scoticus).

Two components of the transmission dynamics of Trichostrongylus tenuis in red grouse are examined and quantified, namely parasite transmission rate and density-dependent reductions in egg production. Age-intensity data for birds of known age suggest that the rate of parasite uptake increases during the first 6 mo of a bird's life and this increase reflects an increase in feeding rate with age and exhibits no signs of self-cure. Analysis of these age-intensity curves permits us to estimate the transmission rate of the free-living infective stages. Reinfection rates of adults treated to reduce parasite intensities were not significantly different from infection rates of naive immature grouse. Secondary infections continued to rise over a period of 18 mo and this suggests that there is no strong host-mediated response against the parasite. Any density-dependent reduction in parasite fecundity is probably very weak and would act through interspecific competition between parasites. Initial analysis of worm egg production in relation to the intensity of worm infection found weak evidence of density-dependent suppression of egg production at high worm intensities. However, a more rigorous analysis found that such a relationship suffered from Type I errors and was a consequence of the aggregated distribution of the parasites. Any density-dependent suppression of parasite egg production is too weak to be detected and would only occur at high worm intensities. The potential density-dependent reductions in fecundity on the population dynamics of T. tenuis and red grouse are examined using a mathematical model. The model suggests that the presence of density-dependent reductions in worm fecundity could produce significant reductions in the propensity of the grouse-nematode system to exhibit population cycles. The sustained cycles observed in the long-term dynamics of the grouse populations in the study area suggest that density-dependent reductions in worm fecundity and establishment are either absent or only operating at levels that are not detectable in field studies.

Human trichostrongyliasis in Queensland.

Trichostrongylus infection, an uncommonly reported zoonosis in Australia, is common in parts of the world where there is close human contact with herbivorous animals. We report 5 cases diagnosed in our laboratory since 1992. Over this period the laboratory has conducted over 46,000 parasitological examinations on feces. All 5 cases were investigated for fecal parasites following detection of a blood eosinophilia. Two of the 5 cases complained of mild abdominal discomfort and diarrhea. It is likely that all obtained their infection following ingestion of contaminated unwashed vegetables which had been fertilized with animal manure. Four of the cases acquired their infection in Queensland and the fifth may have become infected in rural Victoria. All were treated with pyrantel embonate with resolution of the eosinophilia. Follow up fecal specimens showed no parasites. Patients were instructed on the mode of transmission and advised to thoroughly wash any uncooked vegetables prior to ingestion. In our cases, goats and horses were possibly implicated. No published reports of Trichostrongylus spp. in humans in Australia have occurred since the 1930s and it may be more common in Australia than is recognized. The infection may be missed because patients are asymptomatic or have mild gastrointestinal symptoms or only a blood eosinophilia. Trichostrongylus eggs may also be mistaken for hookworm eggs. It is important therefore to distinguish these infections from hookworm infection as the modes of transmission, management and advice regarding prevention differ.

Estimation of uptake of digestive tract strongyle larvae from pasture, using oesophagus fistulated sheep.

Three Merino of Arles ewes fistulated at the oesophagus were used in autumn and spring in order to assess their larval uptake on infected irrigated pasture. The rate of transmission (ingested/available larvae of digestive tract strongyle) was low when the pasture was heavily infected; it was not otherwise modified by environmental factors.

A preliminary investigation into the control of trichostrongylosis in calves in Kenya.

A series of 3 grazing experiments was carried out to collect data relevant for designing techniques to prevent trichostrongylosis in dairy calves in Kenya. In the first experiment 1 week in/5 weeks out rotation was compared with set stocking. The results indicated that rotation is not an effective control measure. In the second experiment the effects of daily removal of faeces from the field were investigated. This practice also had a limited effect in controlling nematode infection in calves. The third experiment concentrated on the influence of nutrition level. It was shown that feeding level does affect the growth rate but its effect on the course of the egg output was not clear-cut. The results also indicated that the dry season greatly reduces herbage infestation.

Seasonal transmission of bovine gastrointestinal nematodes in the Texas Gulf Coast.

Sentinel calves were placed in pastures for 1 month in two environmentally dissimilar areas of the Texas Gulf Coast to determine the seasonal transmission of various gastrointestinal nematodes. Transmission was determined for Cooperia spp, Haemonchus placei, Ostertagia ostertagi, and Trichostrongylus axei. Large numbers of Cooperia spp were acquired from May through November, with the peak of transmission occurring in July and August. Haemonchus placei was encountered on both field sites but was transmitted in large numbers only at one site, during August. Ostertagia ostertagi was acquired primarily from November through May, with the peak of transmission occurring in January and February. January through March was the period when the greatest numbers of Ostertagia larvae undergoing arrested development were acquired. Trichostrongylus axei was abundance in December and January at one field site. In general, trends of transmission were the same in both areas, indicating that weather conditions were most important than vegetation type in larval transmission.

Present status of trichostrongyliasis in Iran.

Infection with species of Trichostrongylus is common among man and animals in most parts of Iran, and human infections with T. orientalis, T. colubriformis, T. vitrinus, T. axei, T. capricola, T. probolurus, T. skrjabini, and a possibly new, unnamed species have been reported. All are found in Isfahan, central Iran, where the overall prevalence is 67% and the predominant species are T. orientalis and T. colubriformis. Among 737 nomads migrating from the central parts to the south, 86% were found to be infected with one or more of five species (in order of frequency): T. colubriformis, T. orientalis, T. axei, T. capricola, and T. vitrinus. In Khuzestan, southwest Iran, human infections with T. orientalis, T. colubriformis, T. axei, and T. vitrinus with an overall prevalence of 71% have been reported. In the northern parts, along the Caspian Sea, the rate is 7% and the species found, in order of frequency, are T. colubriformis, T. axei, T. vitrinus, and T. orientalis. Trichostrongylus infections are also found in the northwest but are rarely seen in the northeast. In most areas females are more frequently and more heavily infected than are males. All species found in man, except the new, unnamed species, are also found in sheep, goats, cattle, and camels; the number of species found and the order of their frequency differ in various animals and in different areas. Infection in other mammals, such as hares (T. retortaeformis and T. orientalis) and porcupines (T. orientalis), has also been reported.